NATIVE NATURAL ENEMIES OF NATIVE WOODBORERS: POTENTIAL AS BIOLOGICAL CONTROL AGENTS FOR THE ASIAN LONGHORNED Michael T. Smith1, Roger W. Fuester1, Joseph M. Tropp1, Ellen M. Aparicio2, Daria Tatman2, and Jeff A. Wildonger2 1USDA Agricultural Research Service, Beneficial Introduction Research Unit 501 South Chapel St., Newark, DE 19713

2Department of Entomology and Wildlife Ecology, University of Delaware Townsend Hall, Newark, DE 19711 ABSTRACT The Asian longhorned beetle (ALB) (Anoplophora including A. glabripennis, A. chinensis, A. nobilis, Apriona glabripennis) is among high-risk invasive species germani, A. swainsoni, Botcera horsfieldi, Chrysobothris that have invaded the U.S. from China. ALB has succudanea, Melanophila decastigma, M. alternatus, attacked 25 deciduous tree species in 13 genera in Trirachys orientalis, Xustrocera globosa, and Xylocopa North America, most notably 7 maple (Acer) species. appendiculata (Qin and Gao 1988). However, it is not Methods developed for control of A. glabripennis clear which of these are indigenous hosts of include the removal of infested trees and the use of D. helophoroides and which are associated only as a result systemic and contact insecticides. However, alternative of evaluations or introductions. environmentally compatible biological control methods 3. Ontsira palliates ()–Reported as a larval are desired. Of particular interest are biological ectoparasitoid of A. chinensis, Callidium villosulum, control agents that possess high host searching ability, S. sinoauster, Metipocregyes rondoni, M. alternatus, particularly under low pest population levels and within S. populnea, and Xustrocera globosa. However, it is not species rich landscapes. Focus is also on egg and early clear which of these are indigenous hosts of O. palliates larval instar life stages of A. glabripennis. and which are associated only as a result of evaluations Two broad approaches are recognized for developing or introductions. O. palliates parasitism is limited to host biological control of invasive species. The first approach larvae feeding within the inner bark, implying that early is based upon natural enemies native to the countries of larval instars may be preferred. origin, and the second approach is based upon natural 4. Zombrus bicolor–Reported as a solitary larval enemies native to the countries of introduction. of many cerambycid and bostrychid wood borers, Based upon the first approach, identified including A. chinensis, Batocera horsfieldi, Ceresium from A. glabripennis or related Anoplophora species in sinicum, Chlorophorus annularis, C. diadema, Desisa China (Chen and He 2006) include: subfasciata, Dere sp., Nadezhdella cantori, Olenecampus 1. guani (Bethylidae)–Reported as octopusitulatus, S. populnea, Semanotus bifasciatus, a larval ectoparasitoid of Monochamus alternatus, S. sinoauster, Trichoferus campestris, and Xylotrechus Saperda populnea, and Semantus sinoauster. S. guani is pyryhoderus (Cerambycidae), and Bostrychopsis parallel reported to control M. alternatus, S. populnea, and Calophagus pekinensis (Bostrychidae). S. sinoauster, and A. chinensis in China, and has been 5. Scleroderma sichuanensis (Bethylidae)–Reported as a evaluated against A. glabripennis and A. chinensis in larval ectoparasitoid of Semanotus sinoauster. Reported to China. control A. chinensis, Clytus validus, M. alternatus, 2. Dastarcus helophoroides (Colydiidae–Reported as S. sinoauster, and S. bifasciatus in China. a larval/pupal ectoparasitoid of 12 cerambycid species,

66 2007 USDA Interagency Research Forum - GTR-NRS-P-28 6. Aprostocetus fukutai ()–Reported as an Based upon the second approach, investigations of natural egg parasitoid of A. chinensis and Apriona germarii enemies native to the countries of introduction were initiated (Liao et al. 1987, Wang and Zhao 1988). in North America at the USDA Agricultural Research Service Beneficial Introduction Research Lab 7. Ontsira anoplophorae sp. nov. (Braconidae–Reported (BIIRU) in 2001 (Smith et al. 2003, 2004). Subsequently, as a gregarious larval ectoparasitoid of A. malasiaca on collaborative studies between BIIRU, University of Illinois, citrus (Yan and Qin 1992, Zhou 1992). and University of Vermont were initiated in 2003 and 2005, 8. Ontsira sp. (Braconidae)–Reported as a larval respectively. These studies focus in large part on species rich parasitoid of A. chinensis (Yan and Qin 1992, Zhou landscapes under low cerambycid population pressure. These 1992). studies have the following three objectives: However, detailed investigations of natural enemies 1. To identify and determine the relative abundance and native to China for biological control of A. glabripennis seasonal occurrence of native cerambycids and associated have focused in large part on S. guani Xiao Wu natural enemy fauna infesting tree species in the Lake States, (: Bethylidae) and D. helophoroides Mid-Atlantic States, and Vermont. Studies have largely (Fairmaire) (Coleoptera: Colydiidae). Both species are focused on known A. glabripennis hosts (e.g., Acer species) ectoparasitoids of a wide range of cerambycid species and species at risk, but have also included tree species that attack either deciduous or coniferous tree species. reported to harbor cerambycids. Investigations and use of these and other potential natural 2. To determine the effects of stress on the relative enemies of A. glabripennis have largely been limited abundance and seasonal occurrence of native cerambycids to highly disturbed landscapes, including windrows and natural enemy fauna. Stress was induced at three levels: bordering agricultural fields, rural roads in agricultural half-girdled trees (girdled 180° around the circumference), areas, monoculture plantations, and street trees in urban fully girdled trees (girdled 360°around the circumference), landscapes, where A. glabripennis is more commonly and felling. undergoing cyclical outbreaks. These landscapes are 3. To evaluate the efficacy of the native natural enemy typically restricted to one or a few tree species, including fauna to parasitize A. glabripennis within infested bolts in Populus (poplar), Salix (willow), Acer (maple), or Ulmus quarantine at BIIRU. (elm), and occasionally Eleagnus angustifolia (Russian- olive). The host searching efficiency ofS. guani and Results reported here focus on BIIRU investigations D. longulus is unknown. Furthermore, their efficacy conducted in forest stands of red maple (Acer rubrum), under A. glabripennis outbreak conditions within pignut hickory (Carya glabra), mockernut hickory (Carya landscapes of limited tree species diversity offers limited tomentosa), and Virginia pine (Pinus virginiana) within insight into their expected efficiency in the U.S., Canada, the Blackbird State Forest in central Delaware. During and Europe, where A. glabripennis population levels are the first year of this multiyear study, trees were stressed low within species rich landscapes. Therefore, before from July 6, 2005, to August 3, 2005. Stressed trees were S. guani and D. longulus can be considered for release inspected on a regular basis from August 2005 to December outside their country of origin, non-target studies are 2006 for signs of colonization (frass, oviposition scars, sap needed. Such non-target studies in the U.S. are awaiting ooze, inner bark sampling). Note that our primary goal, to receipt of import permits for these species. Additional induce colonization by native cerambycids whose natural investigations of native natural enemies of seasonal phenology most resembles A. glabripennis, aimed A. glabripennis within the countries of origin are to obtain the associated natural enemies that might in turn currently focused on non-disturbed natural landscapes parasitize A. glabripennis egg and early larval life stages. where it has long been found attacking native tree species Therefore, at the first sign of colonization, sample bolts under only low pest population levels. (52 cm) were cut from infested trees, returned to BIIRU,

2007 USDA Interagency Research Forum - GTR-NRS-P-28 67 and caged within sono-tubes held in an outdoor insectary. and bark beetle species within infested bolts and with Emergence from each bolt was recorded daily for all insects published literature will establish parasitoid-host until November 2006. Except for potential parasitoids, associations. all insects were preserved for identification. Potential Bioassays parasitoids were bioassayed by caging an individual female , normally together with a single conspecific, To date, most parasitoid species emerging from the on A. glabripennis infested A. rubrum bolts containing 2005 field collected bolts were represented among egg and larval (cambium and xylem) life stages. Bioassay those caged with A. glabripennis infested A. rubrum cages were checked daily for parental mortality and bolts in quarantine. However, among the represented hymenopterous families, the total number of individual emergence of parasitoid F1 offspring. All bioassay bolts were subsequently dissected and all A. glabripennis and parasitoids bioassayed was only 161, 61, and 28 individual parasitoid life stages collected and recorded. parentals originally emerging from hickory, maple, and pine, respectively. Analysis of parental survival (duration),

Cerambycidae parasitization rate, F1 density, and developmental rate has To date, approximately 66% of the pine trees that not yet been completed. However, at least two braconid underwent colonization were among those that had been species, including Atanycolus sp., and one ichneumonid stressed by felling, with the remaining 33% equally divided species were observed displaying parasitization behavior among those that had been stressed by the two girdling on A. glabripennis infested bolts. Among these, only methods. In contrast, nearly 100% of the maple and hickory braconid species were found to successfully parasitize and trees that underwent colonization were among those that complete development of F1’s. Furthermore, the successful had been stressed by felling. Although identifications braconids were largely among those whose natal host are thus far tentative, results indicate that Neoclytus plant was A. rubrum. Subjectively, these results may mucronatus and Xylotrechus colonus, Neoclytus mucronatus indicate natal host plant conditioning among the braconids and Neoclytus a. acuminitas, and Monochamus sp. were the bioassayed. Reciprocal studies will test this hypothesis in most abundant cerambycid species found in C. glabra and an effort to obtain empirical (objective) data. While these C. tomentosa, A. rubrum, and P. virginiana, respectively results are from the first year of a multiyear study and (Table 1). Analysis of the relative seasonal abundance of should be considered as preliminary, these findings are all wood borers and bark has not been completed. significant in that they provide the first concrete evidence However, Monochamus sp. (from pine), Neoclytus a. of a native natural enemy successfully parasitizing acuminitas (from maple), and Neoclytus mucronatus (from A. glabripennis and completing development outside the hickory) each showed a well-defined emergence pattern in countries of origin. early, mid, and late season, respectively. Closing Remarks Parasitoids While results to date are based upon sampling artificial Results also show the relative abundance of parasitoids stress-induced colonized trees, sampling will be expanded belonging to the Braconidae, , and in 2007 to include trees undergoing naturally induced Chacidoidea emerging from C. glabra and C. tomentosa, colonization. Furthermore, while results to date are based A. rubrum, and P. virginiana (Table 2). While many of the upon sampling of only the overwintering generation of cerambycids, braconids, ichneumonids, and Chalcidoidea woodborers and associated natural enemies, sampling have been identified to , they are awaiting species will be expanded in 2007 to include the within season confirmation. Analysis of the relative seasonal abundance generations of woodborers and associated natural enemies. of hymenopterous parasitoids has not been completed. Finally, bioassay methods will be improved in 2007 in an Coupling detailed analysis of associated cerambycid effort to provide more naturally occurring conditions, e.g., environmental conditions.

68 2007 USDA Interagency Research Forum - GTR-NRS-P-28 Table 1. Cerambycid species colonizing (2005) and emerging from (2006) Carya glabra and C. tomentosa, Acer rubrum, and Pinus virginiana. Blackbird State Forest, Delaware. [Tentative Identification]

Tree Species Family/Species Total # Density Insects (#/infested bolt)

Carya glabra & Carya tomentosa Cerambycidae 5,982 20.3 Neoclytus mucronatus 1,759 7.4 Neoclytus a. acuminitas 5 1.3 Neoclytus spp. 6 1.2 Saperda dentatus 345 3.3 Xylotrechus colonus 870 4.7 Cerambycidae spp. 2,988 13.1

Acer rubrum Cerambycidae 137 3.8 Acanthocinus sp. 1 1.0 Aegomorphus modestus 1 1.0 3 1.5 Curius dentatus 2 1.0 Neoclytus mucronatus 20 6.7 Neoclytus a. acuminitas 63 3.9 Cerambycidae spp. 46 2.2

Pinus virginiana Cerambycidae 720 5.1 Astylopsis collari 2 2.0 Astylopsis macula 1 1.0 Monochamus sp. 138 1.7 Neoclytus mucronatus 5 2.5 Neoclytus a. acuminitas 1 1.0 Neoclytus spp. 1 1.0 Xylotrechus colonus 3 1.5 Cerambycidae spp. 569 5.0

Table 2. Hymenoptera parasitoid species colonizing (2005) and emerging from (2006) Carya glabra and C. tomentosa, Acer rubrum, and Pinus virginiana. Blackbird State Forest, Delaware. [Tentative Identification]

Tree Species Family/Species Total # Density Insects (#/infested bolt)

Carya glabra & Carya tomentosa Braconidae 1042 4.1 Ichneumonidae 569 2.7 Chalcidoidea 22 1.4

Acer rubrum Braconidae 115 3.0 Ichneumonidae 41 1.9 Chalcidoidea 10 3.3

Pinus virginiana Braconidae 92 4.4 Ichneumonidae 11 1.8 Chalcidoidea 28 4.7

2007 USDA Interagency Research Forum - GTR-NRS-P-28 69 Literature Cited Wang Yong-jun; Zhao Zi-chen. 1988. A preliminary study on Aprostocetus sp. parasitizing on Apriona Chen, Xue-xin; He, Jun-hua, eds. 2006. Parasitoids germarii (Hope). Kunchongzhishi. 25(6): 347-350. and predators of forest pests in China. USDA Forest Service, Forest Health Technology Enterprise Yan Junjie; QinXixiang. 1992. Anoplophora Team. Beijing, China: China Forestry Publishing glabripennis (Motsch.). In: Xiao Gangrou, ed. House. 216 p. Chinese forest insects: 455-457.

Liao Dingxi; Li Xueliu; Pang Xiongfei; Chen Tailu. Zhou Jiaxi. 1992. Anoplophora nobilis Ganglbauer. 1987. Hymenoptera: Chalcidoidea (1). Economic In: Xiao Gangrou, ed. Chinese forest insects: insect fauna of China Fasc. 34. Beijing, China: 458-459. Science Press. 241 p., 24 plates.

Qin Xixiang; Gao Ruitong. 1988. Dastarcus longulus biological characteristics and its application. Kunchongzhishi. 25(2): 109 112.

Smith, Michael T.; Yang, Zhong-qi; Hérard, Franck; Fuester, Roger; Bauer, Leah; Solter, Leellen; Keena, Melody; D’Amico, Vince. 2003. Biological control of Anoplophora glabripennis (Motsch.): a synthesis of current research programs. In: Fosbroke, S.L.C; Gottschalk, K.W., eds. Proceedings of the U.S. Department of Agriculture interagency research forum on gypsy moth and other invasive species; Annapolis, MD. Newtown Square, PA: U.S. Department of Agriculture, Forest Service, Northeastern Research Station: 87-91.

Smith, Michael T.; Fuester, Roger; Hérard, Franck; Hanks, Larry. 2004. Prospects for inundative release of natural enemies for biological control of Anoplophora glabripennis. In: Fosbroke, S.L.C.; Gottschalk, K.W., eds. Proceedings of the U.S. Department of Agriculture interagency research forum on gypsy moth and other invasive species; Annapolis, MD. Newtown Square, PA: U.S. Department of Agriculture, Forest Service, Northeastern Research Station: 55-61.

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